Developmental transcriptomics of the brittle star Amphiura filiformis reveals gene regulatory network rewiring in echinoderm larval skeleton evolution

Abstract

BackgroundAmongst the echinoderms the class Ophiuroidea is of particular interest for its phylogenetic position, ecological importance and developmental and regenerative biology. However, compared to other echinoderms, notably echinoids (sea urchins), relatively little is known about developmental changes in gene expression in ophiuroids. To address this issue, we have generated and assembled a large RNAseq data set of four key stages of development in the brittle star Amphiura filiformis and a de novo reference transcriptome of comparable quality to that of a model echinoderm—the sea urchin Strongylocentrotus purpuratus. Furthermore, we provide access to the new data via a web interface: http://www.echinonet.eu/shiny/Amphiura_filiformis/.ResultsWe have identified highly conserved genes associated with the development of a biomineralised skeleton. We also identify important class-specific characters, including the independent duplication of the msp130 class of genes in different echinoderm classes and the unique occurrence of spicule matrix (sm) genes in echinoids. Using a new quantification pipeline for our de novo transcriptome, validated with other methodologies, we find major differences between brittle stars and sea urchins in the temporal expression of many transcription factor genes. This divergence in developmental regulatory states is more evident in early stages of development when cell specification begins, rather than when cells initiate differentiation.ConclusionsOur findings indicate that there has been a high degree of gene regulatory network rewiring and clade-specific gene duplication, supporting the hypothesis of a convergent evolution of larval skeleton development in echinoderms.Electronic supplementary materialThe online version of this article (10.1186/s13059-018-1402-8) contains supplementary material, which is available to authorized users.

From genome to anatomy: The architecture and evolution of the skeletogenic gene regulatory network of sea urchins and other echinoderms

“…Indeed, effector gene duplication appears to have been rampant during the evolution of echinoderm biomineralization (Livingston et al, 2006; Adomako-Ankomah and Ettensohn, 2011; Rafiq et al, 2012; Rafiq et al, 2014; Ettensohn, 2014; Ettensohn and Dey, 2017). The flexibility in activation mechanisms described earlier, and the rapid evolution of effector genes, generally support the view that the periphery of a developmental GRN is less constrained than its regulatory core (see also Davidson and Erwin, 2006; Dylus et al, 2018).…”

“…A final insight from comparative studies on the skeletogenic GRN is that effector genes evolve more rapidly than core regulatory machinery. Thus, although a core set of transcription factors has been implicated in skeletogenesis across the phylum, recent transcriptomic and proteomic studies have revealed surprising variation in biomineralization-related effector genes, such as those of the MSP130 and spicule matrix protein families, and point to recent, lineage-specific expansions (Seaver and Livingston, 2015; Flores and Livingston, 2017; Dylus et al, 2018). Indeed, effector gene duplication appears to have been rampant during the evolution of echinoderm biomineralization (Livingston et al, 2006; Adomako-Ankomah and Ettensohn, 2011; Rafiq et al, 2012; Rafiq et al, 2014; Ettensohn, 2014; Ettensohn and Dey, 2017).…”

Transcriptomic data on the transgenerational exposure of the keystone amphipod Gammarus locusta to simvastatin

“…The ORF predictions allowed to produce the second version of transcriptome (2 nd version - Protein coding assembly – All transcripts with ORF (Annex 2)), mainly focused on protein-coding transcripts and using a similar approach to Dylus et al. [12] . Importantly, only 15.61% of the initial transcripts matched coding ORFs with 100 or more amino acids.…”

Cell type phylogenetics informs the evolutionary origin of echinoderm larval skeletogenic cell identity

“…It is still unclear where and how many instances of this heterochronic activation occurred in the echinoderm phylogeny. As the most recent phylogeny of echinoderms places asterozoans (asteroids+ophiuroids) as a sister clade to echinozoans (echinoids+holothurians), it is widely thought that the elaborate larval skeletons in echinoids and ophiuroids are the result of independent evolutionary events 13,19,29,34,35 . Importantly, only recently have developmental gene expression data for holothurians come to light 20 .…”